Comments by Kees de Graaf, March, 2019

At the beginning of my career in the early 1990s we started a project on the effects of sucrose-polyester (olestra), a non-digestible fat substitute that has no caloric value, but has similar oro-sensory properties to fat. We did several studies in humans with a classic preload test-meal design wherein the preloads replaced up to 50 g of fat with 50 g of olestra in realistic food products like croissants, hot rice meals, etc. (Hulshof et al, 1995; de Graaf et al, 1996). With differences of up to 450 kcal in the preloads and study durations of 1 – 12 days, I expected to see large differences after the preloads with respect to feelings of hunger and satiety and energy-intake compensation behavior. However this was not the case. People did not respond at all to the large differences in energy content. Slowly, I realized that the regulation of energy intake in the real world was less precise than I thought. It became clear that the physical and chemical composition of food and their contributions to its sensory properties had an enormous impact on short-term energy intake.

Not long before we carried out our olestra studies, a now-classic paper by Lauren Lissner, David Levitsky and others was published in the American Journal of Clinical Nutrition (Lissner et al., 1987). This study has now been cited more than 400 times and was the first to show that changing the fat content of the daily food supply has a dramatic effect on ad libitum energy intake in humans, not only for one meal or across one day, but also across a period of two weeks. Ad libitum daily energy intakes of diets high in fat (40 – 50% energy) were about 30% higher than of diets low in fat (15 -20%), i.e., about 2700 vs. 2000 kcal/d. Body weight differences of on average 0.8 kg were consistent with changes in energy intakes. One important detail of the study was that the appearance and palatability of the diets were rated similarly, indicating that the higher energy intakes in the high-fat (= high energy density) condition were not caused by higher liking. A few years later, the principal findings of the imprecision of human energy intake regulation were replicated in an 11 week study by Kendal, Levitsky and others (Kendal et al., 1991). The results of these studies had a profound effect on thinking about the role of the everyday food environment on energy intake and body weight, and stimulated extensive research on the role of dietary energy density in moderating daily energy intakes.

In an e-mail exchange, David Levitsky let me know that the idea for the Lissner et al. (1987) study came from earlier observations during his PhD studies that indicated that the degree of overeating after fasting was rather constant and was not affected by the duration of deprivation. In discussions with his mentor George Collier, David came up with the idea that that “human food intake is not controlled by physiological variables such as GI hormones or central neurotransmitters, but rather by environmental variables and habit.” Although this idea contradicted scientific wisdom at the time, it has been supported by many studies of his and others. Certainly, current understanding is that the food environment plays an important role in increasing the prevalence of obesity across the world (Swinburn et al, 1999) .

The initial two studies of Lissner et al. (1987) and Kendall et al. (1991) were done with varying levels of fat in the diet. Since that time, Barbara Rolls and colleagues have shown in an unprecedented series of carefully designed studies how crucial energy density is in moderating daily energy intake (e.g., Rolls et al, 1998). In elegant experiments controlling for the many potential confounding factors in food, Rolls showed over and over again, with realistically designed meals, that higher energy-density diets lead to higher energy intake and increased body weight, whereas lower energy-density diets can support reductions in energy intake and body weight (see Rolls, 2009, for a review). This appears to be true for men and women (e.g. Kral & Rolls, 2004), for overweight and normal-weight people (Rolls et al., 1999), for children and adults (e.g. Kling et al., 2018), and for the short term and long term (e.g. Vernarelli et al., 2018).

Another crucial property of food that has a dramatic effect on ad libitum energy intake is texture. In dozens of studies it has been shown that softer textures can promote higher eating rates and higher energy intakes (e.g. de Graaf, 2012). Liquid calories can easily promote overconsumption, and energy from liquids is poorly compensated later (DiMeglio & Mattes, 2000; Almiron-Roig et al, 2013). It is overwhelmingly clear that not all calories are equal when it comes to human ingestive behavior. Rather, calories have textures and tastes that strongly influence the extent to which they are consumed (McCrickerd & Forde, 2016). From the physiological perspective, the question is how do calories that are consumed faster promote higher energy intakes and calories that are consumed slower support lower energy intakes? One of the potential explanations of the role of texture in satiation is the role of oro-sensory exposure to taste (de Graaf, 2012). Harder textures that lead to longer sensory exposure time to taste result in earlier satiation and lower food intakes (Bolhuis et al, 2014). The suppressive effect of taste exposure on intake has also been shown in studies that controlled for texture, palatability and eating rate (Bolhuis et al, 2011; Weijzen et al. 2009).

Societal debates on obesity, nutrition and health often focus on the reduction of sugar, salt, and fat, and blame the food environment for current global rates of obesity. It is often suggested that targeting the food environment by reducing the availability of so-called “ultra-processed” and “hyper-palatable” foods that may prevent over-consumption. It is clear that food companies compete to maximize the reward value of foods, because these are directly related to choice and intake. Few would argue that food producers should develop unattractive foods that people do not want to eat. One of the great challenges in this respect is to develop foods that people like, but that do not lead to overconsumption.

In the 30 years of progress since Lissner et al.’s.(1987) original demonstration of poor energy compensation for reductions is dietary fat, significant progress has been made in our understanding of how food energy density, texture and sensory properties influence our daily food choices and energy intake. Today a number of research challenges remain, including first and foremost whether lower energy densities, combined with optimal sensory profiles that lower eating rates, can lead to sustained reductions in energy intake and maintenance of healthy body weights. Research aimed at a better understanding the mechanisms behind the imprecise control of energy intake is an important step in this direction.

References

1. Almiron-Roig E, Palla L, Guest K, Ricchiuti C, Vint N, Jebb SA, Drewnowski A. Factors that determine energy compensation: a systematic review of preload studies. Nutrition Reviews. 2013 Jul 1;71(7):458-73.
2. Bolhuis DP, Lakemond CM, de Wijk RA, Luning PA, de Graaf C. Both longer oral sensory exposure to and higher intensity of saltiness decrease ad libitum food intake in healthy normal-weight men. The Journal of Nutrition. 2011 Nov 2;141(12):2242-8.
3. Bolhuis DP, Forde CG, Cheng Y, Xu H, Martin N, de Graaf C. Slow food: sustained impact of harder foods on the reduction in energy intake over the course of the day. PLoS One. 2014 Apr 2;9(4):e93370. de Graaf C. Texture and satiation: the role of oro-sensory exposure time. Physiology & Behavior. 2012 Nov 5;107(4):496-501.
4. de Graaf C, Hulshof T, Weststrate JA, Hautvast JG. Nonabsorbable fat (sucrose polyester) and the regulation of energy intake and body weight. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 1996 Jun 1;270(6):R1386-93.
5. DiMeglio DP, Mattes RD. Liquid versus solid carbohydrate: effects on food intake and body weight. International Journal of Obesity. 2000 Jun;24(6):794.
6. Hulshof T, De Graaf C, Weststrate JA. Short-term satiating effect of the fat replacer sucrose polyester (SPE) in man. British Journal of Nutrition. 1995 Oct;74(4):569-85.
7. Kendall A, Levitsky DA, Strupp BJ, Lissner L. Weight loss on a low-fat diet: consequence of the imprecision of the control of food intake in humans. The American Journal of Clinical Nutrition. 1991 May 1;53(5):1124-9.
8. ling SM, Roe LS, Keller KL, Rolls BJ. Double trouble: Portion size and energy density combine to increase preschool children's lunch intake. Physiology & Behavior. 2016 Aug 1;162:18-26.
9. Kral TV, Rolls BJ. Energy density and portion size: their independent and combined effects on energy intake. Physiology & Behavior. 2004 Aug 1;82(1):131-8.
10. Lissner L, Levitsky DA, Strupp BJ, Kalkwarf HJ, Roe DA. Dietary fat and the regulation of energy intake in human subjects. The American Journal of Clinical Nutrition. 1987 Dec 1;46(6):886-92.
11. McCrickerd K, Forde CG. Sensory influences on food intake control: Moving beyond palatability. Obesity Reviews. 2016 Jan;17(1):18-29.
12. Rolls BJ, Bell EA, Castellanos VH, Chow M, Pelkman CL, Thorwart ML. Energy density but not fat content of foods affected energy intake in lean and obese women. The American Journal of Clinical Nutrition. 1999 May 1;69(5):863-71.
13. Rolls BJ. The relationship between dietary energy density and energy intake. Physiology & Behavior. 2009 Jul 14;97(5):609-15.
14. Swinburn B, Egger G, Raza F. Dissecting obesogenic environments: the development and application of a framework for identifying and prioritizing environmental interventions for obesity. Preventive Medicine 1999 Dec; 29: 563-70.
15. Vernarelli JA, Mitchell DC, Rolls BJ, Hartman TJ. Dietary energy density is associated with obesity and other biomarkers of chronic disease in US adults. European Journal of Nutrition. 2015 Feb 1;54(1):59-65.
16. Weijzen PL, Smeets PA, de Graaf C. Sip size of orangeade: effects on intake and sensory-specific satiation. British Journal of Nutrition. 2009 Oct;102(7):1091-7.